Discovery of a kleptoplastic ‘dinotom’ dinoflagellate and the unique nuclear dynamics of converting kleptoplastids to permanent plastids

Abstract

A monophyletic group of dinoflagellates, called ‘dinotoms’, are known to possess evolutionarily intermediate plastids derived from diatoms. The diatoms maintain their nuclei, mitochondria, and the endoplasmic reticulum in addition with their plastids, while it has been observed that the host dinoflagellates retain the diatoms permanently by controlling diatom karyokinesis. Previously, we showed that dinotoms have repeatedly replaced their diatoms. Here, we show the process of replacements is at two different evolutionary stages in two closely related dinotoms, Durinskia capensis and D. kwazulunatalensis . We clarify that D. capensis is a kleptoplastic protist keeping its diatoms temporarily, only for two months. On the other hand, D. kwazulunatalensis is able to keep several diatoms permanently and exhibits unique dynamics to maintain the diatom nuclei: the nuclei change their morphologies into a complex string-shape alongside the plastids during interphase and these string-shaped nuclei then condense into multiple round nuclei when the host divides. These dynamics have been observed in other dinotoms that possess permanent diatoms, while they have never been observed in any other eukaryotes. We suggest that the establishment of this unique mechanism might be a critical step for dinotoms to be able to convert kleptoplastids into permanent plastids.

Five Non-motile Dinotom Dinoflagellates of the Genus Dinothrix

“…A single cell contained two eukaryotic nuclei: a host dinoflagellate nucleus with condensed chromosomes (dinokaryon) and a small diatom nucleus ( Figures 4G-I). The diatom nucleus changed the morphology from a dispersed string-shape in the interphase (Figure 4G), to a round shape prior to cell division ( Figure 4H), as reported in other dinotoms (Tippit and Pickett-Heaps, 1976;Yamada et al, 2019). The ultrastructure of non-motile cells was typical for dinotoms: in the cytoplasm of the dinoflagellate, a dinokaryon, mitochondria, starch granules, and lipids were observed ( Figure 4I).…”

“…Therefore, each single dinotom cell contains two origins of nuclei, endoplasmic reticulum (ER), Golgi, ribosomes, mitochondria, and plastids, which are derived from either of diatoms or dinoflagellates (Tomas et al, 1973;Jeffery and Vesk, 1976;Horiguchi and Pienaar, 1991), although the dinoflagellate plastids lost the photosynthetic ability (Dodge, 1971;Hehenberger et al, 2014). A dinoflagellate-derived single membrane (symbiosome membrane; Bodył, 2018;Yamada et al, 2019) separates the diatom organelles from the host dinoflagellate cytoplasm. The diatom nucleus, mitochondria, and plastids of dinotoms are transcriptionally active (Imanian and Keeling, 2007;Hehenberger et al, 2014); the diatom nucleus, in particular, remains transcriptionally intact (Hehenberger et al, 2016).…”

“…The second unique property of ODPs is the variety in their origins and evolutionary integration stages: ODPs are derived from at least 14 diatom species (Horiguchi and Takano, 2006;Takano et al, 2008;Čalasan et al, 2017;Yamada et al, 2017). Some ODPs have already evolved into permanently-maintained stages (Tippit and Pickett-Heaps, 1976;Figueroa et al, 2009), while other ODPs remain only temporarily as kleptoplastids, i.e., host dinoflagellates lose ODPs after a time, and need to feed repeatedly on free-living diatoms (Kempton et al, 2002;Yamada et al, 2019). Although it seems that the variation of host dinoflagellates with respect to their habitat environments, life cycles, and diatom preferences is crucial for understanding the evolutionary processes of the ODPs, many dinotoms, with the exception of Durinskia cf.…”

Genomic Insights into Plastid Evolution

“…To date, there is only one known example of a kleptoplasty-derived dinotom. In this case, the dinoflagellate Durinskia capensis appears to retain its diatom only temporarily, for ∼2 months, and does not appear to control its cell division ( Yamada et al. 2019 ).…”

Changes in the transcriptome, ploidy, and optimal light intensity of a cryptomonad upon integration into a kleptoplastic dinoflagellate

“…In contrast, the nucleus of algal prey is temporally retained with the kleptoplast in other species, including the ciliate Mesodinium rubrum , some dinoflagellates, the katablepharid Hatena arenicola . In addition, among the dinoflagellates Durinskia spp., Durinskia capensis temporally retains the kleptoplast and nucleus of a diatom prey, whereas two other species permanently retain diatom cells in which the diatom nucleus and chloroplasts divide in accordance with the cell division of the dinoflagellate host [ 14 , 15 ]. The retention of the endosymbiont nucleus and the chloroplast division in accord with the host cell cycle are also observed in cryptophytes and chlorarachniophytes, which possess bona fide chloroplasts with a vestigial nucleus of red and green algal origin, respectively, but with a greatly reduced genome size [ 16 , 17 ].…”